Abstract

Zinc oxide (ZnO) nanoparticles (NPs) are widely used in cosmetic and sunscreen products which are applied topically to the skin. Despite their widespread use, the safety and biological response of these particles remains an active area of investigation. In this paper we present methods based on in vivo multiphoton microscopy (MPM) in skin to address relevant questions about the potential toxicity and immunological response of ZnO NPs. Registration of time-lapse volumetric MPM images allows the same skin site to be tracked across multiple days for visualizing and quantifying cellular and structural changes in response to NP exposure. Making use of the unique optical properties of ZnO enables high contrast detection of the NPs in the presence of strong autofluorescence and second harmonic generation (SHG) background from the skin. A green fluorescent protein (GFP) bone marrow (BM) transplanted mouse model is used to visualize and assess the dynamic response of BM-derived immune cells. These cells are visualized to assess the potential for ZnO NPs to interact with immune cells and elicit an immune reaction in skin. We investigate both topical and dermal exposure of the ZnO NPs. The methods and findings presented in this paper demonstrate a novel approach for tracking ZnO NPs in vivo and for visualizing the cellular response of the exposed tissue to assess the immunological response and potential toxicity of these particles.

© 2013 OSA

Full Article  |  PDF Article

References

  • View by:
  • |
  • |
  • |

  1. M. D. Newman, M. Stotland, and J. I. Ellis, “The safety of nanosized particles in titanium dioxide- and zinc oxide-based sunscreens,” J. Am. Acad. Dermatol.61(4), 685–692 (2009).
    [CrossRef] [PubMed]
  2. H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
    [CrossRef]
  3. H. A. Jeng and J. Swanson, “Toxicity of metal oxide nanoparticles in mammalian cells,” J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng.41(12), 2699–2711 (2006).
    [CrossRef]
  4. S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
    [CrossRef] [PubMed]
  5. A. O. Gamer, E. Leibold, and B. van Ravenzwaay, “The in vitro absorption of microfine zinc oxide and titanium dioxide through porcine skin,” Toxicol. In Vitro20(3), 301–307 (2006).
    [CrossRef] [PubMed]
  6. E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).
  7. B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
    [CrossRef] [PubMed]
  8. L. W. Zhang and N. A. Monteiro-Riviere, “Assessment of quantum dot penetration into intact, tape-stripped, abraded and flexed rat skin,” Skin Pharmacol. Physiol.21(3), 166–180 (2008).
    [CrossRef] [PubMed]
  9. J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
    [CrossRef] [PubMed]
  10. M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
    [CrossRef] [PubMed]
  11. S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
    [CrossRef] [PubMed]
  12. N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
    [CrossRef] [PubMed]
  13. C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
    [CrossRef] [PubMed]
  14. J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
    [CrossRef] [PubMed]
  15. NANODERM, “Quality of skin as a barrier to ultra-fine particles. final report.,” Project Number: QLK4-CT-2002–02678 (2007).
  16. J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
    [CrossRef] [PubMed]
  17. A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
    [CrossRef] [PubMed]
  18. W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
    [CrossRef] [PubMed]
  19. B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J.72(6), 2405–2412 (1997).
    [CrossRef] [PubMed]
  20. K. Koenig and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8(3), 432–439 (2003).
    [CrossRef] [PubMed]
  21. B. W. Graf and S. A. Boppart, “Multimodal in vivo skin imaging with integrated optical coherence and multiphoton microscopy,” IEEE J. Sel. Top. Quantum Electron.18(4), 1280–1286 (2012).
    [CrossRef]
  22. K. König, “Clinical multiphoton tomography,” J Biophotonics1(1), 13–23 (2008).
    [CrossRef] [PubMed]
  23. B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
    [CrossRef]
  24. S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
    [CrossRef]
  25. D. C. Dai, S. J. Xu, S. L. Shi, M. H. Xie, and C. M. Che, “Efficient multiphoton-absorption-induced luminescence in single-crystalline ZnO at room temperature,” Opt. Lett.30(24), 3377–3379 (2005).
    [CrossRef] [PubMed]
  26. A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
    [CrossRef] [PubMed]
  27. M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
    [CrossRef] [PubMed]
  28. Z. Song, T. A. Kelf, W. H. Sanchez, M. S. Roberts, J. Rička, M. Frenz, and A. V. Zvyagin, “Characterization of optical properties of ZnO nanoparticles for quantitative imaging of transdermal transport,” Biomed. Opt. Express2(12), 3321–3333 (2011).
    [CrossRef] [PubMed]
  29. L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
    [CrossRef] [PubMed]
  30. B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.
  31. R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
    [CrossRef] [PubMed]
  32. J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
    [CrossRef] [PubMed]
  33. H. G. Breunig, H. Studier, and K. König, “Multiphoton excitation characteristics of cellular fluorophores of human skin in vivo,” Opt. Express18(8), 7857–7871 (2010).
    [CrossRef] [PubMed]

2012 (1)

B. W. Graf and S. A. Boppart, “Multimodal in vivo skin imaging with integrated optical coherence and multiphoton microscopy,” IEEE J. Sel. Top. Quantum Electron.18(4), 1280–1286 (2012).
[CrossRef]

2011 (3)

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Z. Song, T. A. Kelf, W. H. Sanchez, M. S. Roberts, J. Rička, M. Frenz, and A. V. Zvyagin, “Characterization of optical properties of ZnO nanoparticles for quantitative imaging of transdermal transport,” Biomed. Opt. Express2(12), 3321–3333 (2011).
[CrossRef] [PubMed]

2010 (3)

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

H. G. Breunig, H. Studier, and K. König, “Multiphoton excitation characteristics of cellular fluorophores of human skin in vivo,” Opt. Express18(8), 7857–7871 (2010).
[CrossRef] [PubMed]

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

2009 (4)

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

M. D. Newman, M. Stotland, and J. I. Ellis, “The safety of nanosized particles in titanium dioxide- and zinc oxide-based sunscreens,” J. Am. Acad. Dermatol.61(4), 685–692 (2009).
[CrossRef] [PubMed]

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

2008 (4)

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

K. König, “Clinical multiphoton tomography,” J Biophotonics1(1), 13–23 (2008).
[CrossRef] [PubMed]

L. W. Zhang and N. A. Monteiro-Riviere, “Assessment of quantum dot penetration into intact, tape-stripped, abraded and flexed rat skin,” Skin Pharmacol. Physiol.21(3), 166–180 (2008).
[CrossRef] [PubMed]

2007 (4)

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

2006 (3)

A. O. Gamer, E. Leibold, and B. van Ravenzwaay, “The in vitro absorption of microfine zinc oxide and titanium dioxide through porcine skin,” Toxicol. In Vitro20(3), 301–307 (2006).
[CrossRef] [PubMed]

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

H. A. Jeng and J. Swanson, “Toxicity of metal oxide nanoparticles in mammalian cells,” J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng.41(12), 2699–2711 (2006).
[CrossRef]

2005 (1)

2004 (2)

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

2003 (1)

K. Koenig and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8(3), 432–439 (2003).
[CrossRef] [PubMed]

2002 (1)

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

1999 (1)

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

1997 (2)

B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J.72(6), 2405–2412 (1997).
[CrossRef] [PubMed]

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Adami, G.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Adie, S. G.

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Aguer, P.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Alitalo, K.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Baik, J. E.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Barberet, P.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Barbotteau, Y.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Barron, A. R.

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

Barthelmes, H.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Bawendi, M. G.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Becker, W.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Biswas, M.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

Bitar, R.

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

Bock, M.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

Boppart, M. D.

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Boppart, S. A.

B. W. Graf and S. A. Boppart, “Multimodal in vivo skin imaging with integrated optical coherence and multiphoton microscopy,” IEEE J. Sel. Top. Quantum Electron.18(4), 1280–1286 (2012).
[CrossRef]

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Bovenzi, M.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Breunig, H. G.

Breusing, M.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

Butler, M. K.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Byrne, D.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

Casey, P.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Chaney, E. J.

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Che, C. M.

Cohn, L. H.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Colvin, V. L.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Cozart, C. R.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Crosera, M.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Cross, S. E.

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

Dai, D. C.

Das, S. K.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

De Grand, A. M.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

De Lisio, M.

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Denk, W.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Dor, D. M.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Ellis, J. I.

M. D. Newman, M. Stotland, and J. I. Ellis, “The safety of nanosized particles in titanium dioxide- and zinc oxide-based sunscreens,” J. Am. Acad. Dermatol.61(4), 685–692 (2009).
[CrossRef] [PubMed]

Filon Larese, F.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Florio, C.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Frangioni, J. V.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Frenz, M.

Gamer, A. O.

A. O. Gamer, E. Leibold, and B. van Ravenzwaay, “The in vitro absorption of microfine zinc oxide and titanium dioxide through porcine skin,” Toxicol. In Vitro20(3), 301–307 (2006).
[CrossRef] [PubMed]

Gärtner, E.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Gers-Barlag, H.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Gierden, A.

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

Gomez, L.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Gontier, E.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Gopee, N. V.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Graf, B. W.

B. W. Graf and S. A. Boppart, “Multimodal in vivo skin imaging with integrated optical coherence and multiphoton microscopy,” IEEE J. Sel. Top. Quantum Electron.18(4), 1280–1286 (2012).
[CrossRef]

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Gratton, E.

B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J.72(6), 2405–2412 (1997).
[CrossRef] [PubMed]

Greenoak, G.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Grice, J. E.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Grunwald, R.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

Gulson, B.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Habchi, C.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Han, S. H.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Hanley, C.

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Hanna, C.

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Hidaka, H.

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

Hohenberg, H.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Howard, P. C.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Incerti, S.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Innes, B.

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

Jang, C.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Jeng, H. A.

H. A. Jeng and J. Swanson, “Toxicity of metal oxide nanoparticles in mammalian cells,” J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng.41(12), 2699–2711 (2006).
[CrossRef]

Jones, J. J.

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

Jung, K.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Kataru, R. P.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Kelf, T. A.

Kim, S.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Kinsley, L.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Kobayashi, H.

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

Koenig, K.

K. Koenig and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8(3), 432–439 (2003).
[CrossRef] [PubMed]

Koh, G. Y.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Koike, T.

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

König, K.

Korsch, M.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Lademann, J.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Laurence, R. G.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Lee, J.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Leibold, E.

A. O. Gamer, E. Leibold, and B. van Ravenzwaay, “The in vitro absorption of microfine zinc oxide and titanium dioxide through porcine skin,” Toxicol. In Vitro20(3), 301–307 (2006).
[CrossRef] [PubMed]

Lejeune, O.

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

Lim, Y. T.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Lin, L. L.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Maina, G.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Marjanovic, M.

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Masters, B. R.

B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J.72(6), 2405–2412 (1997).
[CrossRef] [PubMed]

Mavon, A.

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

McCall, M.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

McCormick, P.

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

McCulloch, M.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

McGilvray, I. D.

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

McGlynn, E.

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

Mihaljevic, T.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Miquel, C.

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

Monteiro-Riviere, N. A.

L. W. Zhang and N. A. Monteiro-Riviere, “Assessment of quantum dot penetration into intact, tape-stripped, abraded and flexed rat skin,” Skin Pharmacol. Physiol.21(3), 166–180 (2008).
[CrossRef] [PubMed]

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

Moretto, P.

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Mueller, G.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Nakayama, A.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Nathens, A. B.

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

Newman, M. D.

M. D. Newman, M. Stotland, and J. I. Ellis, “The safety of nanosized particles in titanium dioxide- and zinc oxide-based sunscreens,” J. Am. Acad. Dermatol.61(4), 685–692 (2009).
[CrossRef] [PubMed]

Oytam, Y.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Parker, J. A.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Payre, B.

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

Pfeiffer, S.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Pflücker, F.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Pouthier, T.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Prow, T. W.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Punnoose, A.

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Ricka, J.

Rickmeyer, C.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Riemann, I.

K. Koenig and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8(3), 432–439 (2003).
[CrossRef] [PubMed]

Roberts, D. W.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Roberts, M. J.

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Roberts, M. S.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Z. Song, T. A. Kelf, W. H. Sanchez, M. S. Roberts, J. Rička, M. Frenz, and A. V. Zvyagin, “Characterization of optical properties of ZnO nanoparticles for quantitative imaging of transdermal transport,” Biomed. Opt. Express2(12), 3321–3333 (2011).
[CrossRef] [PubMed]

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

Robertson, T. A.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

Ross, J. A.

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

Rotstein, O. D.

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

Rouse, J. G.

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

Ryman-Rasmussen, J. P.

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

Sanchez, W.

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Sanchez, W. H.

Sato, T.

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

Schaefer, H.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Schulz, J.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Schwendener, R. A.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Serpone, N.

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

Shi, S. L.

Siitonen, P. H.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

So, P. T. C.

B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J.72(6), 2405–2412 (1997).
[CrossRef] [PubMed]

Soltesz, E. G.

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Song, Z.

Soyer, H. P.

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Sterry, W.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Stotland, M.

M. D. Newman, M. Stotland, and J. I. Ellis, “The safety of nanosized particles in titanium dioxide- and zinc oxide-based sunscreens,” J. Am. Acad. Dermatol.61(4), 685–692 (2009).
[CrossRef] [PubMed]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Studier, H.

Surleve-Bazeille, J. E.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Swanson, J.

H. A. Jeng and J. Swanson, “Toxicity of metal oxide nanoparticles in mammalian cells,” J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng.41(12), 2699–2711 (2006).
[CrossRef]

Taylor, A.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Thörling, C.

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Thurber, A.

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Trotter, J.

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

Tsuzuki, T.

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

Valero, M. C.

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

van Ravenzwaay, B.

A. O. Gamer, E. Leibold, and B. van Ravenzwaay, “The in vitro absorption of microfine zinc oxide and titanium dioxide through porcine skin,” Toxicol. In Vitro20(3), 301–307 (2006).
[CrossRef] [PubMed]

Walker, N. J.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Warbritton, A. R.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Webb, P.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Webb, W. W.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Weigmann, H. J.

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Wendel, V.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Wepf, R.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Will, T.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Wingett, D. G.

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Wittern, K. P.

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Xie, M. H.

Xu, S. J.

Yang, H.

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

Yang, J. Z.

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

Ynsa, M. D.

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

Yu, W. W.

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Zanette, C.

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

Zhang, J.

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Zhang, L. W.

L. W. Zhang and N. A. Monteiro-Riviere, “Assessment of quantum dot penetration into intact, tape-stripped, abraded and flexed rat skin,” Skin Pharmacol. Physiol.21(3), 166–180 (2008).
[CrossRef] [PubMed]

Zhao, X.

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Zou, Y. H.

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Zvyagin, A. V.

Z. Song, T. A. Kelf, W. H. Sanchez, M. S. Roberts, J. Rička, M. Frenz, and A. V. Zvyagin, “Characterization of optical properties of ZnO nanoparticles for quantitative imaging of transdermal transport,” Biomed. Opt. Express2(12), 3321–3333 (2011).
[CrossRef] [PubMed]

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

Adv. Drug Deliv. Rev. (1)

J. Schulz, H. Hohenberg, F. Pflücker, E. Gärtner, T. Will, S. Pfeiffer, R. Wepf, V. Wendel, H. Gers-Barlag, and K. P. Wittern, “Distribution of sunscreens on skin,” Adv. Drug Deliv. Rev.54(Suppl 1), S157–S163 (2002).
[CrossRef] [PubMed]

Arch. Surg. (1)

J. J. Jones, I. D. McGilvray, A. B. Nathens, R. Bitar, and O. D. Rotstein, “Glutathione depletion prevents lipopolysaccharide-induced local skin inflammation,” Arch. Surg.132(11), 1165–1169, discussion 1170 (1997).
[CrossRef] [PubMed]

Biomed. Opt. Express (1)

Biophys. J. (1)

B. R. Masters, P. T. C. So, and E. Gratton, “Multiphoton excitation fluorescence microscopy and spectroscopy of in vivo human skin,” Biophys. J.72(6), 2405–2412 (1997).
[CrossRef] [PubMed]

Blood (1)

R. P. Kataru, K. Jung, C. Jang, H. Yang, R. A. Schwendener, J. E. Baik, S. H. Han, K. Alitalo, and G. Y. Koh, “Critical role of CD11b(+) macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution,” Blood113(22), 5650–5659 (2009).
[CrossRef] [PubMed]

IEEE J. Sel. Top. Quantum Electron. (1)

B. W. Graf and S. A. Boppart, “Multimodal in vivo skin imaging with integrated optical coherence and multiphoton microscopy,” IEEE J. Sel. Top. Quantum Electron.18(4), 1280–1286 (2012).
[CrossRef]

Int. Arch. Occup. Environ. Health (1)

M. Crosera, M. Bovenzi, G. Maina, G. Adami, C. Zanette, C. Florio, and F. Filon Larese, “Nanoparticle dermal absorption and toxicity: a review of the literature,” Int. Arch. Occup. Environ. Health82(9), 1043–1055 (2009).
[CrossRef] [PubMed]

J Biophotonics (2)

K. König, “Clinical multiphoton tomography,” J Biophotonics1(1), 13–23 (2008).
[CrossRef] [PubMed]

M. S. Roberts, M. J. Roberts, T. A. Robertson, W. Sanchez, C. Thörling, Y. H. Zou, X. Zhao, W. Becker, and A. V. Zvyagin, “In vitro and in vivo imaging of xenobiotic transport in human skin and in the rat liver,” J Biophotonics1(6), 478–493 (2008).
[CrossRef] [PubMed]

J. Am. Acad. Dermatol. (1)

M. D. Newman, M. Stotland, and J. I. Ellis, “The safety of nanosized particles in titanium dioxide- and zinc oxide-based sunscreens,” J. Am. Acad. Dermatol.61(4), 685–692 (2009).
[CrossRef] [PubMed]

J. Appl. Phys. (1)

S. K. Das, M. Biswas, D. Byrne, M. Bock, E. McGlynn, M. Breusing, and R. Grunwald, “Multiphoton-absorption induced ultraviolet luminescence of ZnO nanorods using low-energy femtosecond pulses,” J. Appl. Phys.108(4), 043107 (2010).
[CrossRef]

J. Biomed. Opt. (2)

A. V. Zvyagin, X. Zhao, A. Gierden, W. Sanchez, J. A. Ross, and M. S. Roberts, “Imaging of zinc oxide nanoparticle penetration in human skin in vitro and in vivo,” J. Biomed. Opt.13(6), 064031 (2008).
[CrossRef] [PubMed]

K. Koenig and I. Riemann, “High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution,” J. Biomed. Opt.8(3), 432–439 (2003).
[CrossRef] [PubMed]

J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng. (1)

H. A. Jeng and J. Swanson, “Toxicity of metal oxide nanoparticles in mammalian cells,” J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng.41(12), 2699–2711 (2006).
[CrossRef]

J. Invest. Dermatol. (1)

E. Gontier, C. Habchi, T. Pouthier, P. Aguer, P. Barberet, Y. Barbotteau, S. Incerti, M. D. Ynsa, J. E. Surleve-Bazeille, and P. Moretto, “Nuclear microscopy and electron microscopy studies of percutaneous penetration of nanoparticles in mammalian skin,” J. Invest. Dermatol.123, (2004).

J. Oleo Sci. (1)

H. Hidaka, H. Kobayashi, T. Koike, T. Sato, and N. Serpone, “DNA damage photoinduced by cosmetic pigments and sunscreen agents under solar exposure and artificial UV illumination,” J. Oleo Sci.55(5), 249–261 (2006).
[CrossRef]

Nano Lett. (1)

J. G. Rouse, J. Z. Yang, J. P. Ryman-Rasmussen, A. R. Barron, and N. A. Monteiro-Riviere, “Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin,” Nano Lett.7(1), 155–160 (2007).
[CrossRef] [PubMed]

Nanoscale Res. Lett. (1)

C. Hanley, A. Thurber, C. Hanna, A. Punnoose, J. Zhang, and D. G. Wingett, “The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction,” Nanoscale Res. Lett.4(12), 1409–1420 (2009).
[CrossRef] [PubMed]

Nat. Biotechnol. (1)

S. Kim, Y. T. Lim, E. G. Soltesz, A. M. De Grand, J. Lee, A. Nakayama, J. A. Parker, T. Mihaljevic, R. G. Laurence, D. M. Dor, L. H. Cohn, M. G. Bawendi, and J. V. Frangioni, “Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping,” Nat. Biotechnol.22(1), 93–97 (2004).
[CrossRef] [PubMed]

Opt. Express (1)

Opt. Lett. (1)

Pharm. Res. (1)

L. L. Lin, J. E. Grice, M. K. Butler, A. V. Zvyagin, W. Becker, T. A. Robertson, H. P. Soyer, M. S. Roberts, and T. W. Prow, “Time-correlated single photon counting for simultaneous monitoring of zinc oxide nanoparticles and NAD(P)H in intact and barrier-disrupted volunteer skin,” Pharm. Res.28(11), 2920–2930 (2011).
[CrossRef] [PubMed]

Proc. SPIE (1)

B. W. Graf, M. C. Valero, E. J. Chaney, M. Marjanovic, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal microscopy for tracking cell dynamics in live tissue,” Proc. SPIE7902, 790206, 790206-8 (2011).
[CrossRef]

Science (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science248(4951), 73–76 (1990).
[CrossRef] [PubMed]

Skin Pharmacol. Appl. Skin Physiol. (1)

J. Lademann, H. J. Weigmann, C. Rickmeyer, H. Barthelmes, H. Schaefer, G. Mueller, and W. Sterry, “Penetration of titanium dioxide microparticles in a sunscreen formulation into the horny layer and the follicular orifice,” Skin Pharmacol. Appl. Skin Physiol.12(5), 247–256 (1999).
[CrossRef] [PubMed]

Skin Pharmacol. Physiol. (3)

A. Mavon, C. Miquel, O. Lejeune, B. Payre, and P. Moretto, “In vitro percutaneous absorption and in vivo stratum corneum distribution of an organic and a mineral sunscreen,” Skin Pharmacol. Physiol.20(1), 10–20 (2007).
[CrossRef] [PubMed]

L. W. Zhang and N. A. Monteiro-Riviere, “Assessment of quantum dot penetration into intact, tape-stripped, abraded and flexed rat skin,” Skin Pharmacol. Physiol.21(3), 166–180 (2008).
[CrossRef] [PubMed]

S. E. Cross, B. Innes, M. S. Roberts, T. Tsuzuki, T. A. Robertson, and P. McCormick, “Human skin penetration of sunscreen nanoparticles: In-vitro assessment of a novel micronized zinc oxide formulation,” Skin Pharmacol. Physiol.20(3), 148–154 (2007).
[CrossRef] [PubMed]

Technology (1)

B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, and S. A. Boppart, “Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin,” Technology. In Press.

Toxicol. In Vitro (1)

A. O. Gamer, E. Leibold, and B. van Ravenzwaay, “The in vitro absorption of microfine zinc oxide and titanium dioxide through porcine skin,” Toxicol. In Vitro20(3), 301–307 (2006).
[CrossRef] [PubMed]

Toxicol. Sci. (2)

B. Gulson, M. McCall, M. Korsch, L. Gomez, P. Casey, Y. Oytam, A. Taylor, M. McCulloch, J. Trotter, L. Kinsley, and G. Greenoak, “Small amounts of zinc from zinc oxide particles in sunscreens applied outdoors are absorbed through human skin,” Toxicol. Sci.118(1), 140–149 (2010).
[CrossRef] [PubMed]

N. V. Gopee, D. W. Roberts, P. Webb, C. R. Cozart, P. H. Siitonen, A. R. Warbritton, W. W. Yu, V. L. Colvin, N. J. Walker, and P. C. Howard, “Migration of intradermally injected quantum dots to sentinel organs in mice,” Toxicol. Sci.98(1), 249–257 (2007).
[CrossRef] [PubMed]

Other (1)

NANODERM, “Quality of skin as a barrier to ultra-fine particles. final report.,” Project Number: QLK4-CT-2002–02678 (2007).

Cited By

OSA participates in CrossRef's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (6)

Fig. 1
Fig. 1

In vivo MPM imaging of GFP bone marrow transplanted mouse skin. High resolution renderings of (A) SHG and (B) TPEF image volumes. SHG images visualize the collagen network in the dermis and TPEF images show individual BM-derived cells. Dark circular features in the SHG images indicated by red arrows are hair follicles. Wide area mosaics of the skin based on (C) SHG, (D) TPEF and (E) multimodal overlays to show spatial correspondence. In vivo imaging allows the density of BM-derived cells and spatial positions within the skin to be non-invasively assessed. The BM derived cells in the skin are a heterogeneous population including several different types of immune cells, including macrophages, neutrophils and dendritic cells. Scale bars are 300 µm.

Fig. 2
Fig. 2

In vivo imaging of BM-derived GFP cell dynamics in skin during an immune reaction. (A, B) SHG, (C, D) TPEF and (E, F) overlaid en face sections of in vivo mouse skin (A, C, E) before and (B, D, F) 24 hours after a linear incision and exposure to lipopolysaccharide (LPS). Intensity scaling of the GFP images in (C) and (D) are the same in order to demonstrate the large increase in GFP signal. (G) Overlaid en face section 24 hours after the wound with the intensity scale of the GFP image adjusted to allow the cellular features of the GFP signal to be seen. (H) A higher magnification en face section of the region marked by the red box in (G) showing individual GFP cells. Scale bar for (A-G) is 300 µm and 100 µm for (H).

Fig. 3
Fig. 3

Imaging zinc-oxide (ZnO) nanoparticles in the presence of skin auto-fluorescence based on SHG and TPL. (A, B) SHG channel, (C, D) TPL channel and (E, F) merged channels from in vivo mouse skin images following a linear incision and (A, C, E) ZnO particle exposure or (B, D, F) a control without particles. ZnO particles generate both SHG (red arrow) and TPL (green arrow) and thus merging the two channels discriminates ZnO particles from autofluorescence background which only appears in the TPL channel. Scale bar is 300 µm.

Fig. 4
Fig. 4

Time-lapse in vivo imaging of mouse skin following topical exposure to ZnO NPs. The MPM signal due to ZnO particles is evident following the exposure (red arrow) and gradually reduces over the 48 hours time period. No significant increase in the GFP signal is observed, indicating no immune response was caused by the presence of the ZnO NPs. Scale bar is 500 µm.

Fig. 5
Fig. 5

Time-lapse in vivo imaging of mouse skin following a linear incision and dermal exposure to (A) ZnO NPs and (B) a control treatment of water. The accumulation of the ZnO particles in the incision (red arrow) and their persistence over the 48 hour time period is apparent. The ZnO images from the control treatment contains a weak autofluorescence signal (yellow arrow). In both the ZnO exposure and the control, the GFP signal does not significantly increase by 24 hours after the treatment and only slightly increases by 48 hours. This suggests that the exposure to ZnO NPs does not result in a significantly increased inflammatory response compared to the control treatment. Scale bar is 300 µm.

Fig. 6
Fig. 6

(A) Quantitative plots of the total GFP signal intensity within the time-lapse image volumes demonstrates that neither topical exposure or dermal exposure of ZnO NPs has elicited a strong immune response. Magnified en face sections of the incision sites for (B) ZnO dermal exposure at 48 hours, (C) control dermal treatment at 48 hours and the (D) positive control LPS exposure at 24 hours. The lack of any cellular features in (B) and (C) compared to (D) suggests that this GFP signal is due to a strong auto fluorescence from the wound site and not BM-derived GFP cells. Scale bar is 100 µm.

Metrics